Outputs and executive functions of the Mauthner neuron

The Mauthner neuron has monosynaptic connections with many of the spinal motor neurons that it excites; a short collateral of the Mauthner axon makes contact with a special region of the motor axon several micrometres from the cell body (see Fig. 3.8b). A spike in the Mauthner axon produces an EPSP in the motor neuron with a synaptic delay of about 0.6 ms, so the transmission is probably chemical. The excitation of a substantial number of other motor neurons is relayed by way of a premotor interneuron and so involves a slightly greater delay. The motor axons travel a relatively short distance to the trunk muscles, where they have normal chemically transmitting synaptic endings on the muscle surface. This short and direct pathway is responsible for the short delay of about 2 ms between a Mauthner neuron spike and the onset of a spike in the trunk muscles (see Fig. 3.9 b, c).

A spike in the Mauthner axon inhibits the spinal motor neurons contralateral to the axon at the same time as it excites those ipsilateral to the axon. The inhibition appears to be mediated by inhibitory interneurons that cross the midline and are activated by electrical synapses from the Mauthner axon (Fig. 3.11a). This crossed inhibitory circuit makes sure that, if only a short interval in time separates spikes in the left and right Mauthner neurons, only the earlier of the two Mauthner spikes is able to fire its motor neurons. If the two Mauthner neurons spike simultaneously, the crossed inhibition prevents any motor output at all.

Within the brain, branches from the axon of the Mauthner neuron excite a number of cranial relay neurons, which carry out some important

Interneuron

Figure 3.11 Output circuitry of the Mauthner neuron. (a) Neuronal circuit generating excitation and inhibition of spinal motor neurons, showing: the Mauthner neuron (M); spinal relay neurons (SR); crossed inhibitory interneuron (CI); and spinal motor neurons (SMo). Chemical excitatory (—O, electrical excitatory (—|) and chemical inhibitory (—•) synapses are shown. (b) Neuronal circuit generating excitation of the cranial motor neurons and self-inhibition, showing the Mauthner neuron (M); cranial relay neuron (CR); cranial motor neurons (CMo); and the Mauthner inhibitor (MI). Synaptic symbols are as in (a), plus electrical inhibition of the axon cap (—®|).

Figure 3.11 Output circuitry of the Mauthner neuron. (a) Neuronal circuit generating excitation and inhibition of spinal motor neurons, showing: the Mauthner neuron (M); spinal relay neurons (SR); crossed inhibitory interneuron (CI); and spinal motor neurons (SMo). Chemical excitatory (—O, electrical excitatory (—|) and chemical inhibitory (—•) synapses are shown. (b) Neuronal circuit generating excitation of the cranial motor neurons and self-inhibition, showing the Mauthner neuron (M); cranial relay neuron (CR); cranial motor neurons (CMo); and the Mauthner inhibitor (MI). Synaptic symbols are as in (a), plus electrical inhibition of the axon cap (—®|).

functions in the startle response (Fig. 3.11 b). The cranial relay neurons excite motor neurons of muscles that close the jaw and draw in the eyes, which helps to streamline the fish for its escape. In addition, the cranial relay neurons monosynaptically excite a group of interneurons that inhibit both the Mauthner neurons.

These Mauthner inhibitors have cell bodies clustered around the ventral dendrite and they act to inhibit the Mauthner neuron in several ways. Some of them exert an unusual form of electrical inhibition: they have axons coiled tightly round the origin of the Mauthner axon, contributing to the axon cap (see Fig. 3.8b). When spikes are generated in these axons, they make the outside of the Mauthner neuron locally more positive, which has the same effect as driving the intracellular potential more negative. Spikes from these neurons thus exert a kind of brief stranglehold on the Mauthner neuron, right at the zone where its spikes are initiated. This electrical inhi bition follows a Mauthner spike with a delay of about 1 ms and so prevents the Mauthner neuron from firing twice in response to a given stimulus. Furthermore, the cranial relay neurons are excited by branches of both left and right Mauthner axons, with the result that the contralateral Mauthner neuron also receives electrical inhibition with the same short delay after a spike in the ipsilateral axon.

The electrical inhibition of both Mauthner neurons is a brief event, lasting no more than about 2 ms, but it is followed by inhibition through chemical synapses that lasts much longer. The Mauthner inhibitors produce this inhibition through their axon terminals on the cell body of the Mauthner neuron, which make conventional chemical synapses. The chemical inhibition begins about 1 ms after the electrical inhibition, and lasts for about 45 ms, which takes it well into the second stage of the startle response. There is evidence that this direct inhibition is backed up by pre-synaptic inhibitory synapses made by the Mauthner inhibitors on to the synaptic terminals of the sensory neurons on the Mauthner neuron dendrites, and also by separate inhibitory circuits that are activated directly by the sensory neurons. The result of these inhibitory mechanisms is not only that the active Mauthner neuron and its contralateral partner are shut down as soon as a spike has been generated, but also that they are kept shut down long enough for the startle response to go to completion.

Although the involvement of Mauthner neurons in triggering startle responses in teleost fish is clear, this does not mean that this is the only function that these neurons serve. Sudden lunges by goldfish to capture prey on the water surface involve movements similar to those of a startle response, and follow a Mauthner neuron spike (Canfield & Rose, 1993). Besides integrating information about a source of potential danger, a Mauthner neuron must be able to collect information that triggers an attack at the appropriate time. The input and output circuitry of a Mauthner neuron is arranged so that it can initiate and co-ordinate a rapid, directed movement.

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